Dressed for sex: red as a female sexual signal in humans

Background

In many non-human primate species, a display of red by a female serves as a sexual signal to attract male conspecifics. Red is associated with sex and romance in humans, and women convey their sexual interest to men through a variety of verbal, postural, and behavioral means. In the present research, we investigate whether female red ornamentation in non-human primates has a human analog, whereby women use a behavioral display of red to signal their sexual interest to men.

Methodology/Principal Findings

Three studies tested the hypothesis that women use red clothing to communicate sexual interest to men in profile pictures on dating websites. In Study 1, women who imagined being interested in casual sex were more likely to display red (but not other colors) on their anticipated web profile picture. In Study 2, women who indicated interest in casual sex were more likely to prominently display red (but not other colors) on their actual web profile picture. In Study 3, women on a website dedicated to facilitating casual sexual relationships were more likely to prominently exhibit red (but not other colors) than women on a website dedicated to facilitating marital relationships.

Conclusions/Significance

These results establish a provocative parallel between women and non-human female primates in red signal coloration in the mating game. This research shows, for the first time, a functional use of color in women''s sexual self-presentation, and highlights the need to extend research on color beyond physics, physiology, and preference to psychological functioning.     

Sexual selection and trichromatic color vision in primates: statistical support for the preexisting-bias hypothesis

The evolution of trichromatic color vision in primates may improve foraging performance as well as intraspecific communication; however, the context in which color vision initially evolved is unknown. We statistically examined the hypothesis that trichromatic color vision in primates represents a preexisting bias for the evolution of red coloration (pelage and/or skin) through sexual selection. Our analyses show that trichromatic color vision evolved before red pelage and red skin, as well as before gregarious mating systems that would promote sexual selection for visual traits and other forms of intraspecific communication via red traits. We also determined that both red pelage and red skin were more likely to evolve in the presence of color vision and mating systems that promote sexual selection. These results provide statistical support for the hypothesis that trichromatic color vision in primates evolved in a context other than intraspecific communication with red traits, most likely foraging performance, but, once evolved, represented a preexisting bias that promoted the evolution of red traits through sexual selection.     

Red is not a proxy signal for female genitalia in humans

Red is a colour that induces physiological and psychological effects in humans, affecting competitive and sporting success, signalling and enhancing male social dominance. The colour is also associated with increased sexual attractiveness, such that women associated with red objects or contexts are regarded as more desirable. It has been proposed that human males have a biological predisposition towards the colour red such that it is 'sexually salient'. This hypothesis argues that women use the colour red to announce impending ovulation and sexual proceptivity, with this functioning as a proxy signal for genital colour, and that men show increased attraction in consequence. In the first test of this hypothesis, we show that contrary to the hypothesis, heterosexual men did not prefer redder female genitalia and, by extension, that red is not a proxy signal for genital colour. We found a relative preference for pinker genital images with redder genitalia rated significantly less sexually attractive. This effect was independent of raters' prior sexual experience and variation in female genital morphology. Our results refute the hypothesis that men's attraction to red is linked to an implied relationship to genital colour and women's signalling of fertility and sexual proceptivity.     

Opsin expression predicts male nuptial color in threespine stickleback

Theoretical models of sexual selection suggest that male courtship signals can evolve through the build‐up of genetic correlations between the male signal and female preference. When preference is mediated via increased sensitivity of the signal characteristics, correlations between male signal and perception/sensitivity are expected. When signal expression is limited to males, we would expect to find signal‐sensitivity correlations in males. Here, we document such a correlation within a breeding population of threespine stickleback mediated by differences in opsin expression. Males with redder nuptial coloration express more long‐wavelength‐sensitive (LWS) opsin, making them more sensitive to orange and red. This correlation is not an artifact of shared tuning to the optical microhabitat. Such correlations are an essential feature of many models of sexual selection, and our results highlight the potential importance of opsin expression variation as a substrate for signal‐preference evolution. Finally, these results suggest a potential sensory mechanism that could drive negative frequency‐dependent selection via male–male competition and thus maintain variation in male nuptial color.     

Sex differences in main olfactory system pathways involved in psychosexual function

We summarize literature from animal and human studies assessing sex differences in the ability of the main olfactory system to detect and process sex‐specific olfactory signals (“pheromones”) that control the expression of psychosexual functions in males and females. A case is made in non primate mammals for an obligatory role of pheromonal signaling via the main olfactory system (in addition to the vomeronasal‐accessory olfactory system) in mate recognition and sexual arousal, with male‐specific as well as female‐specific pheromones subserving these functions in the opposite sex. Although the case for an obligatory role of pheromones in mate recognition and mating among old world primates, including humans, is weaker, we review the current literature assessing the role of putative human pheromones (eg, AND, EST, “copulin”), detected by the main olfactory system, in promoting mate choice and mating in men and women. Based on animal studies, we hypothesize that sexually dimorphic effects of putative human pheromones are mediated via main olfactory inputs to the medial amygdala which, in turn, transmits olfactory information to sites in the hypothalamus that regulate reproduction.     

No compelling positive association between ovarian hormones and wearing red clothing when using multinomial analyses

Several studies report that wearing red clothing enhances women's attractiveness and signals sexual proceptivity to men. The associated hypothesis that women will choose to wear red clothing when fertility is highest, however, has received mixed support from empirical studies. One possible cause of these mixed findings may be methodological. The current study aimed to replicate recent findings suggesting a positive association between hormonal profiles associated with high fertility (high estradiol to progesterone ratios) and the likelihood of wearing red. We compared the effect of the estradiol to progesterone ratio on the probability of wearing: red versus non-red (binary logistic regression); red versus neutral, black, blue, green, orange, multi-color, and gray (multinomial logistic regression); and each of these same colors in separate binary models (e.g., green versus non-green). Red versus non-red analyses showed a positive trend between a high estradiol to progesterone ratio and wearing red, but the effect only arose for younger women and was not robust across samples. We found no compelling evidence for ovarian hormones increasing the probability of wearing red in the other analyses. However, we did find that the probability of wearing neutral was positively associated with the estradiol to progesterone ratio, though the effect did not reach conventional levels of statistical significance. Findings suggest that although ovarian hormones may affect younger women's preference for red clothing under some conditions, the effect is not robust when differentiating amongst other colors of clothing. In addition, the effect of ovarian hormones on clothing color preference may not be specific to the color red.     

Face perception is modulated by sexual preference

Face perception is mediated by a distributed neural system in the human brain . The response to faces is modulated by cognitive factors such as attention, visual imagery, and emotion ; however, the effects of gender and sexual orientation are currently unknown. We used fMRI to test whether subjects would respond more to their sexually preferred faces and predicted such modulation in the reward circuitry. Forty heterosexual and homosexual men and women viewed photographs of male and female faces and assessed facial attractiveness. Regardless of their gender and sexual orientation, all subjects similarly rated the attractiveness of both male and female faces. Within multiple, bilateral face-selective regions in the visual cortex, limbic system, and prefrontal cortex, similar patterns of activation were found in all subjects in response to both male and female faces. Consistent with our hypothesis, we found a significant interaction between stimulus gender and the sexual preference of the subject in the thalamus and medial orbitofrontal cortex, where heterosexual men and homosexual women responded more to female faces and heterosexual women and homosexual men responded more to male faces. Our findings suggest that sexual preference modulates face-evoked activation in the reward circuitry.     

Musical improvisation skill in a prospective partner is associated with mate value and preferences,consistent with sexual selection and parental investment theory: Implications for the origin of music

Music is a human universal, which suggests a biological adaptation. Several evolutionary explanations have been proposed, covering the entire spectrum of natural, sexual, and group selection. Here we consider the hypothesis that musical behaviour constitutes a reliable or even costly signal of fitness, and thus may have evolved as a human trait through sexual selection. We experimentally tested how musical performance quality (MPQ), in improvisations on the drums, saxophone, and violin, affects mate values and mate preferences perceived by a prospective partner. Swedish student participants (27 of each sex) saw a face of a person of the opposite sex and heard a piece of improvised music being played. The music occurred in three levels of MPQ and the faces in three levels of facial attractiveness (FA). For each parametric combination of MPG and FA, the participants rated four mate value scales (intelligence, health, social status, and parenting skill) and four mate preference scales (date, intercourse, and short- and long term relationship). Consistent with sexual selection theory, mate value ratings were generally increased by MPQ for raters of both sexes. Consistent with more specific hypotheses that follow from combining sexual selection and parental investment theory, women’s but not men’s preference for a long-term, but not short-term, relationship was significantly increased by MPQ, MPQ generally affected women’s ratings more than men’s, FA generally affected men’s ratings more than women’s, and women’s ratings of intelligence were even more influenced by MPQ than by FA.     

Winter Plumage Coloration in Male American Goldfinches: Do Reduced Ornaments Serve Signaling Functions in the Non‐Breeding Season?

The signaling role of sexual ornaments that are displayed during the mating season is well known for many species, but dimorphisms that occur in the non‐breeding season have received much less attention, particularly when individuals only partially express their breeding condition during reproductively inactive periods. I assessed variation in the expression of colorful breeding and non‐breeding plumages in male American goldfinches (Carduelis tristis), a species in which males molt out of their colorful breeding ornaments in the fall but still display reduced carotenoid‐ and melanin‐based sexual dichromatism during the winter. I found that variability in the saturation of carotenoid‐based plumage pigmentation did not differ significantly between the breeding and non‐breeding seasons. Moreover, the area of melanin coloration in the cap was more variable in winter than when it is fully displayed during breeding. I also detected a significant positive correlation between the extent of melanin coloration during the winter and the saturation of non‐breeding carotenoid‐based plumage. Because of such variation in and correlated expression of these two color ornaments in winter, it is conceivable that male goldfinches display these hints of non‐breeding coloration for use as conspecific social or sexual signals. Natural selection pressures like predation and energetic demands are traditionally thought of as factors that restrict sex ornaments to breeding times alone, but this should not preclude animals from simply reducing their exaggerated features during winter and finding an expression optimum that balances signal costs and value. Such ‘remnant’ winter ornaments might be expected to evolve not only in animals that live in large non‐breeding groups (e.g. status‐signaling systems) but also in those where mates begin associating before breeding onset.     

Patterns of MHC‐dependent mate selection in humans and nonhuman primates: a meta‐analysis

Genes of the major histocompatibility complex (MHC) in vertebrates are integral for effective adaptive immune response and are associated with sexual selection. Evidence from a range of vertebrates supports MHC‐based preference for diverse and dissimilar mating partners, but evidence from human mate choice studies has been disparate and controversial. Methodologies and sampling peculiarities specific to human studies make it difficult to know whether wide discrepancies in results among human populations are real or artefact. To better understand what processes may affect MHC‐mediated mate choice across humans and nonhuman primates, we performed phylogenetically controlled meta‐analyses using 58 effect sizes from 30 studies across seven primate species. Primates showed a general trend favouring more MHC‐diverse mates, which was statistically significant for humans. In contrast, there was no tendency for MHC‐dissimilar mate choice, and for humans, we observed effect sizes indicating selection of both MHC‐dissimilar and MHC‐similar mates. Focusing on MHC‐similar effect sizes only, we found evidence that preference for MHC similarity was an artefact of population ethnic heterogeneity in observational studies but not among experimental studies with more control over sociocultural biases. This suggests that human assortative mating biases may be responsible for some patterns of MHC‐based mate choice. Additionally, the overall effect sizes of primate MHC‐based mating preferences are relatively weak (Fisher's Z correlation coefficient for dissimilarity Zr = 0.044, diversity Zr = 0.153), calling for careful sampling design in future studies. Overall, our results indicate that preference for more MHC‐diverse mates is significant for humans and likely conserved across primates.     

What do men want? Re-examining whether men benefit from higher fertility than is optimal for women

Several empirical observations suggest that when women have more autonomy over their reproductive decisions, fertility is lower. Some evolutionary theorists have interpreted this as evidence for sexual conflicts of interest, arguing that higher fertility is more adaptive for men than women. We suggest the assumptions underlying these arguments are problematic: assuming that women suffer higher costs of reproduction than men neglects the (different) costs of reproduction for men; the assumption that men can repartner is often false. We use simple models to illustrate that (i) men or women can prefer longer interbirth intervals (IBIs), (ii) if men can only partner with wives sequentially they may favour shorter IBIs than women, but such a strategy would only be optimal for a few men who can repartner. This suggests that an evolved universal male preference for higher fertility than women prefer is implausible and is unlikely to fully account for the empirical data. This further implies that if women have more reproductive autonomy, populations should grow, not decline. More precise theoretical explanations with clearly stated assumptions, and data that better address both ultimate fitness consequences and proximate psychological motivations, are needed to understand under which conditions sexual conflict over reproductive timing should arise.     

The Function of Mounting Behaviour in Farmed Red Deer Calves

The function of mounting behaviour was studied in farmed red deer (Cervus elaphus) calves. On the basis of previous work, we tested two alternative hypotheses about the function of this behaviour. The first hypothesis deals with the proximate function of the behaviour. Three predictions were tested: (1a) mounting behaviour attracts the attention of the mother and/or consolidates the mother–calf bond; (1b) mounting is intended to obtain more milk; (1c) mounting is intended to prevent other calves from sucking from the mother. The second hypothesis deals with an ultimate function in practising for future life with two predictions tested: (2a) mounting behaviour is part of calves' play behaviour promoting development of the calf's locomotor and social skills; (2b) calves gain sexual experience through mounting behaviour. For the study, 50 hind‐calf pairs were observed. The maternity of individual hinds was confirmed by a genetical analysis. The hinds were classified as ‘maternal’ and ‘non‐maternal’ and the calves as ‘filial’ and ‘non‐filial’. We recorded 40 cases of mounting behaviour involving 25 hinds and 21 calves. Our results suggest that the mounting behaviour of red deer calves serves several different functions depending on the circumstances. In association with suckling, calves of both sexes mounted maternal hinds mainly to attract their attention and to achieve another suckling. In situations not associated with suckling, mounting by male calves might be considered part of their sexual training. On the other hand, mounting by female calves probably reflects the attempt to maintain contact with their mother in tense situations.     

Sexual selection of multiple handicaps in the red-collared widowbird: female choice of tail length but not carotenoid display

Although sexual selection through female choice explains exaggerated male ornaments in many species, the evolution of the multicomponent nature of most sexual displays remains poorly understood. Theoretical models suggest that handicap signaling should converge on a single most informative quality indicator, whereas additional signals are more likely to be arbitrary Fisherian traits, amplifiers, or exploitations of receiver psychology. Male nuptial plumage in the highly polygynous red-collared widowbird (Euplectes ardens) comprises two of the commonly advocated quality advertisements (handicaps) in birds: a long graduated tail and red carotenoid coloration. Here we use multivariate selection analysis to investigate female choice in relation to male tail length, color (reflectance) of the collar, other aspects of morphology, ectoparasite load, display rate, and territory quality. The order and total number of active nests obtained are used as measures of male reproductive success. We demonstrate a strong female preference and net sexual selection for long tails, but marginal or no effects of color, morphology, or territory quality. Tail length explained 47% of male reproductive success, an unusually strong fitness effect of natural ornament variation. Fluctuating tail asymmetry was unrelated to tail length, and had no impact on mating success. For the red collar, there was negative net selection on collar area, presumably via its negative relationship with tail length. None of the color variables (hue, chroma, and brightness) had significant selection differentials, but a partial effect (selection gradient) of chroma might represent a color preference when tail length is controlled for. We suggest that the red collar functions in male agonistic interactions, which has been strongly supported by subsequent work. Thus, female choice targets only one handicap, extreme tail elongation, disregarding or even selecting against the carotenoid display. We discuss whether long tails might be better indicators of genetic quality than carotenoid pigmentation. As regards the evolution of multiple ornaments, we propose that multiple handicap signaling is stable not because of multiple messages but because of multiple receivers, in this case females and males.     

Preferences for masculinity in male bodies change across the menstrual cycle

In human females cyclic shifts in preference have been documented for odour and physical and behavioral male traits. Women prefer the smell of dominant males, more masculine male faces and men behaving more dominantly when at peak fertility than at other times in their menstrual cycle. Here we examine variation in preferences for body sexual dimorphism. Across two studies, both between- and within-participant, we show that women prefer greater masculinity in male bodies at times when their fertility is likely highest, in the follicular phase of their cycle. Shifts were seen when rating for a short-term but not when rating for a long-term relationship. In line with studies showing similar effects for facial sexual dimorphism, we also show that women prefer greater masculinity when they think themselves attractive than when they think themselves less attractive. These results indicate that women's preferences for sexual dimorphism in male bodies follow a similar pattern as found for sexual dimorphism and dominance in other domains and such differences in preference may serve a similar function. Cyclic preferences could influence women to select partners when most likely to become pregnant that possess traits that may be most likely to maximize their offspring's quality via attraction to masculinity or serve to help acquire investment via attraction to femininity.     

Female Sexual Preferences Toward Conspecific and Hybrid Male Mating Calls in Two Species of Polygynous Deer, <Emphasis Type="Italic">Cervus elaphu</Emphasis>s and <Emphasis Type="Italic">C. nippon</Emphasis>

The behavioral processes at the basis of hybridization and introgression are understudied in terrestrial mammals. We use a unique model to test the role of sexual signals as a reproductive barrier to introgression by investigating behavioral responses to male sexual calls in estrous females of two naturally allopatric but reproductively compatible deer species, red deer and sika deer. Previous studies demonstrated asymmetries in acoustic species discrimination between these species: most but not all female red deer prefer conspecific over sika deer male calls while female sika deer exhibit no preference differences. Here, we extend this examination of acoustic species discrimination to the role of male sexual calls in introgression between parent species and hybrids. Using two-speaker playback experiments, we compared the preference responses of estrous female red and sika deer to male sexual calls from conspecifics versus red × sika hybrids. These playbacks simulate early secondary contact between previously allopatric species after hybridization has occurred. Based on previous conspecific versus heterospecific playbacks, we predicted that most female red deer would prefer conspecific calls while female sika deer would show no difference in their preference behaviors toward conspecific and hybrid calls. However, results show that previous asymmetries did not persist as neither species exhibited more preferences for conspecific over hybrid calls. Thus, vocal behavior is not likely to deter introgression between these species during the early stages of sympatry. On a wider scale, weak discrimination against hybrid sexual signals could substantially contribute to this important evolutionary process in mammals and other taxa.     

Conspicuous Female Ornamentation and Tests of Male Mate Preference in Threespine Sticklebacks (Gasterosteus aculeatus)

Sexual selection drives the evolution of exaggerated male ornaments in many animal species. Female ornamentation is now acknowledged also to be common but is generally less well understood. One example is the recently documented red female throat coloration in some threespine stickleback (Gasterosteus aculeatus) populations. Although female sticklebacks often exhibit a preference for red male throat coloration, the possibility of sexual selection on female coloration has been little studied. Using sequential and simultaneous mate choice trials, we examined male mate preferences for female throat color, as well as pelvic spine color and standard length, using wild-captured threespine sticklebacks from the Little Campbell River, British Columbia. In a multivariate analysis, we found no evidence for a population-level mate preference in males, suggesting the absence of directional sexual selection on these traits arising from male mate choice. Significant variation was detected among males in their preference functions, but this appeared to arise from differences in their mean responsiveness across mating trials and not from variation in the strength (i.e., slope) of their preference, suggesting the absence of individual-level preferences as well. When presented with conspecific intruder males, male response decreased as intruder red throat coloration increased, suggesting that males can discriminate color and other aspects of phenotype in our experiment and that males may use these traits in intrasexual interactions. The results presented here are the first to explicitly address male preference for female throat color in threespine sticklebacks.     

SEXUAL SELECTION CAN INCREASE THE EFFECT OF RANDOM GENETIC DRIFT—A QUANTITATIVE GENETIC MODEL OF POLYMORPHISM IN OOPHAGA PUMILIO,THE STRAWBERRY POISON‐DART FROG

The variation in color pattern between populations of the poison‐dart frog Oophaga pumilio across the Bocas del Toro archipelago in Panama is suggested to be due to sexual selection, as two other nonsexually selecting Dendrobatid species found in the same habitat and range do not exhibit this variation. We theoretically test this assertion using a quantitative genetic sexual selection model incorporating aposematic coloration and random drift. We find that sexual selection could cause the observed variation via a novel process we call “coupled drift.” Within our model, for certain parameter values, sexual selection forces frog color to closely follow the evolution of female preference. Any between‐population variation in preference due to genetic drift is passed on to color. If female preference in O. pumilio is strongly affected by drift, whereas color in the nonsexually selecting Dendrobatid species is not, coupled drift will cause increased between‐population phenotypic variation. However, with different parameter values, coupled drift will result in between‐population variation in color being suppressed compared to its neutral value, or in little or no effect. We suggest that coupled drift is a novel theoretical process that could have a role linking sexual selection with speciation both in O. pumilio, and perhaps more generally.     

Is there a link between paternity concern and female genital cutting in West Africa?

Here we explore the relationship between female genital cutting (FGC), sexual behaviour, and marriage opportunities in five West African countries. Using large demographic datasets (n 72,438 women, 12,704 men, 10,695 couples) we explore key (but untested) assumptions of an evolutionary proposal that FGC persists because it provides evolutionary fitness benefits for men by reducing non-paternity rates. We identify and test three assumptions implicit in this proposal. We test whether cut women have reduced extra-pair sex before or within marriage; whether FGC is associated with a younger age at marriage as an indication of partner preference; and whether individual and group-level indicators of paternity concern are associated with a stronger preference for marriage to women with FGC.Our results show that FGC status does not affect the odds of women engaging in several indicators of premarital sex, however women with FGC have significantly lower odds of having more than one lifetime sexual partner. We also show that women with FGC get married at a younger age which supports the argument that FGC status influences women's marriage opportunities, even when it does not restrict sexual activity. Finally, we find that in population groups where reported sexual activity and perceived risk of women's extra-pair sex is high, men have higher odds of marrying a first wife with FGC. Together, these results indicate that paternity certainty may be one of several factors contributing to the persistence of FGC in this sample, and that group-level sexual norms are key to maintaining the practice of FGC through the marriage market.     

The benefits of costly signaling: Meriam turtle hunters

Hunting, particularly when it involves large game that is extensivelyshared, has been suggested to serve as a form of costly signalingby hunters, serving to attract mates and allies or to detercompetitors. Empirical evidence presented elsewhere on turtlehunting practiced by Meriam people of Torres Strait, Australia,supports several key predictions of the costly signaling account.Here we present evidence from the same study bearing on anotherkey prediction, that signalers (hunters) gain social and reproductivebenefits. Specifically, we find that successful hunters gainsocial recognition, have an earlier onset of reproduction, achievehigher age-specific reproductive success, and gain higher qualitymates, who also achieve above-average reproductive success.Meriam hunters also average more mates (women who bear theiroffspring) and more co-resident sexual partners than other men,and these partners (but not mates) are significantly younger.Several lines of evidence thus support the idea that huntingis a form of costly signaling in this population. Alternativehypotheses involving reciprocity (from grateful recipients ofmeat) and direct offspring provisioning by hunters are not consistentwith available evidence, but in the absence of experimentalmanipulation we cannot rule out a role for phenotypic correlation.     

The function and mechanism of vocal accommodation in humans and other primates

The study of non‐human animals, in particular primates, can provide essential insights into language evolution. A critical element of language is vocal production learning, i.e. learning how to produce calls. In contrast to other lineages such as songbirds, vocal production learning of completely new signals is strikingly rare in non‐human primates. An increasing body of research, however, suggests that various species of non‐human primates engage in vocal accommodation and adjust the structure of their calls in response to environmental noise or conspecific vocalizations. To date it is unclear what role vocal accommodation may have played in language evolution, in particular because it summarizes a variety of heterogeneous phenomena which are potentially achieved by different mechanisms. In contrast to non‐human primates, accommodation research in humans has a long tradition in psychology and linguistics. Based on theoretical models from these research traditions, we provide a new framework which allows comparing instances of accommodation across species, and studying them according to their underlying mechanism and ultimate biological function. We found that at the mechanistic level, many cases of accommodation can be explained with an automatic perception–production link, but some instances arguably require higher levels of vocal control. Functionally, both human and non‐human primates use social accommodation to signal social closeness or social distance to a partner or social group. Together, this indicates that not only some vocal control, but also the communicative function of vocal accommodation to signal social closeness and distance must have evolved prior to the emergence of language, rather than being the result of it. Vocal accommodation as found in other primates has thus endowed our ancestors with pre‐adaptations that may have paved the way for language evolution.